Phylogenomics resolves the relationships among Hydrophiloidea-Histeroidea families (Coleoptera) and challenges the single colonization of aquatic habitats

Abstract

Beetle superfamilies Histeroidea and Hydrophiloidea form a well-supported monophylum with c. 9000 described species, but the relationships among the families remain unresolved, hindering the studies of the early evolution of the group. This study presents the first genomic data for all modern families, including the first genomes for Synteliidae, Sphaeritidae, Georissidae and Epimetopidae. Using datasets of 4215, 1100 and 709 protein-coding genes, we reconstructed the relationships among the families, reconfirmed the Early Triassic split of Hydrophiloidea and Histeroidea, and revealed the Early to Middle Jurassic origin of modern families. All datasets and analytical methods revealed the same topology for Hydrophiloidea. The superfamily consists of two main clades: the helophorid lineage (Georissidae + Helophoridae + Hydrochidae) and the hydrophilid lineage (Epimetopidae + Spercheidae + Hydrophilidae), with Helophoridae + Hydrochidae and Spercheidae + Hydrophilidae as strongly supported clades; the riparian Georissidae and Epimetopidae form early branching clades in each lineage. In Histeroidea, we detected a significant conflict in phylogenetic signal, indicating a more complex and dynamic molecular evolution than in Hydrophiloidea: our analyses reject Synteliidae as sister to Histeridae but are not decisive on whether Synteliidae are sister to Sphaeritidae or to all other Histeroidea. The reconstruction of habitat preferences indicated that ancestral Hydrophiloidea inhabited moist substrates at the sides of lakes or rivers but were not aquatic. Aquatic habitats were colonized twice independently: once by Helophoridae + Hydrochidae and once by an ancestor of Spercheidae + Hydrophilidae. We discuss the evidence for and against this novel Riparian Ancestor Hypothesis in detail.